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Estimating C4 photosynthesis parameters by fitting intensive A/Ci curves

Abstract

Measurements of photosynthetic assimilation rate as a function of intercellular CO2 (A/Ci curves) are widely used to estimate photosynthetic parameters for C3 species, yet few parameters have been reported for C4 plants, because of a lack of estimation methods. Here, we extend the framework of widely used estimation methods for C3 plants to build estimation tools by exclusively fitting intensive A/Ci curves (6–8 more sampling points) for C4 using three versions of photosynthesis models with different assumptions about carbonic anhydrase processes and ATP distribution. We use simulation analysis, out of sample tests, existing in vitro measurements and chlorophyll-fluorescence measurements to validate the new estimation methods. Of the five/six photosynthetic parameters obtained, sensitivity analyses show that maximal-Rubisco-carboxylation-rate, electron-transport-rate, maximal-PEP-carboxylation-rate, and carbonic-anhydrase were robust to variation in the input parameters, while day respiration and mesophyll conductance varied. Our method provides a way to estimate carbonic anhydrase activity, a new parameter, from A/Ci curves, yet also shows that models that do not explicitly consider carbonic anhydrase yield approximate results. The two photosynthesis models, differing in whether ATP could freely transport between RuBP and PEP regeneration processes yielded consistent results under high light, but they may diverge under low light intensities. Modeling results show selection for Rubisco of low specificity and high catalytic rate, low leakage of bundle sheath, and high PEPC affinity, which may further increase C4 efficiency.

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Abbreviations

a :

Light absorptance of leaf

A c :

Rubisco carboxylation assimilation rate

RCPC :

RuBP carboxylation and PEPc carboxylation limitation assimilation

RrPc :

RuBP regeneration and PEP carboxylation limitation assimilation

A g :

Gross CO2 assimilation rate per unit leaf area

A j :

RuBP regeneration assimilation rate

A n :

Net CO2 assimilation rate per unit leaf area

RcPr :

RuBP carboxylation and PEPc regeneration limitation assimilation

RrPr :

RuBP regeneration and PEPc regeneration limitation assimilation

α:

The fraction of O2 evolution occurring in the bundle sheath

c :

Scaling constant for temperature dependence for parameters

CaL :

Lower boundary CO2 under which assimilation is limited by RuBP carboxylation and PEPc carboxylation

CaH :

Higher boundary CO2 above which assimilation is limited by RuBP regeneration and PEPc regeneration

C bs :

Bundle sheath CO2 concentration

C i :

Intercellular CO2 concentration

C m :

Mesophyll CO2 concentration

ΔH a :

Energy of activation for temperature dependence for parameters

ΔH d :

Energy of deactivation for temperature dependence for parameters

ΔS :

Entropy for temperature dependence for parameters

\(\phi_{{_{\text{PSII}} }}\) :

Quantum yield

γ*(25):

The specificity of Rubisco at 25 °C

g bs :

Bundle sheath conductance for CO2

g bso :

Bundle sheath conductance for O2

g m :

Mesophyll conductance for CO2

I :

Light intensity

J(25):

Maximum rate of electron transport at 25 °C at a specific light intensity

J max(25):

Maximum rate of electron transport at 25 °C

K c(25):

Michaelis–Menten constant of Rubisco activity for CO2 at 25 °C

K o(25):

Michaelis–Menten constants of Rubisco activity for O2

K p(25):

Michaelis–Menten constants of PEP carboxylation for CO2

O bs :

O2 concentration in the bundle sheath cells

Q10 for K p :

Temperature sensitivity parameter for Kp

R :

The molar gas constant

R d :

Daytime respiration

R dbs :

Daytime respiration in bundle sheath cells

R dm :

Daytime respiration in mesophyll cells

Rubisco:

Ribulose-1,5-bisphosphate carboxylase/oxygenase

RuBP:

Ribulose-1,5-bisphosphate

T k :

Leaf absolute temperature

V c :

Velocity of Rubisco carboxylation

V cmax(25):

Maximal velocity of Rubisco carboxylation at 25 °C

V p :

PEP carboxylation

V pc :

PEPc reaction rate

V pmax(25):

Maximal PEP carboxylation rate at 25 °C

V pr :

PEP regeneration rate

x :

The maximal ratio of total electron transport could be used for PEP carboxylation

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Acknowledgements

We are grateful for support from the University of Pennsylvania. We thank Dr. Jesse Nippert, Kansas State University, for providing the fluorometer chamber.

Funding

We sincerely thank the constructive comments from two anonymous reviewers. The experiments are supported by Department Research Fund (to H.Z.) from Department of Biology, University of Pennsylvania.

Author information

Correspondence to Haoran Zhou.

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Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (XLSX 56 KB) Supplementary Material I. Deriving C4 photosynthesis parameters by fitting A/Ci curves for model without carbonic anhydrase reaction using Sharkey’s fitting procedure.

Supplementary material 2 (XLSX 67 KB) Supplementary Material II. Deriving C4 photosynthesis parameters by fitting A/Ci curves for model without carbonic anhydrase reaction using Yin’s fitting procedure.

Supplementary material 3 (XLSX 59 KB) Supplementary Material III. Deriving C4 photosynthesis parameters by fitting A/Ci curves for model with carbonic anhydrase reaction using Sharkey’s fitting procedure.

Supplementary material 4 (DOCX 26768 KB) Supplementary Material IV. Estimation results for two estimation methods of with/without carbonic anhydrase reaction for nine species (using Supplementary Material I and III).

Supplementary material 5 (XLSX 34 KB) Supplementary Material V. Instruction for use and set the solver macro.

Supplementary material 6 (XLSX 49 KB) Supplementary Material VI. Resources and data for Temperature dependence of input and output parameters.

Supplementary material 7 (DOCX 156 KB) Supplementary Methods, Tables and Figures.

Supplementary material 8 (R 10 KB) C4Estimation 0.1.tar.gz is the R package which contains estimation methods for model with and without carbonic anhydrase reaction using Sharkey and Yin’s fitting procedures (same with Supplementary Material I, II and III) and three additional methods in which researchers can provide new temperature response parameters further.

Supplementary material 9 (RD 2 KB)

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Supplementary material 12 (3D 9 KB)

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Supplementary material 16 (RWL 11 KB)

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Zhou, H., Akçay, E. & Helliker, B.R. Estimating C4 photosynthesis parameters by fitting intensive A/Ci curves. Photosynth Res 141, 181–194 (2019). https://doi.org/10.1007/s11120-019-00619-8

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Keywords

  • A/C i curves
  • C4
  • Estimation method
  • Non-linear curve fitting
  • Photosynthesis parameters
  • V cmax
  • Electron transport
  • PEP carboxylation rate
  • Carbonic anhydrase